22
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Root exudates drive the soil-borne legacy of aboveground pathogen infection

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          Background

          Plants are capable of building up beneficial rhizosphere communities as is evidenced by disease-suppressive soils. However, it is not known how and why soil bacterial communities are impacted by plant exposure to foliar pathogens and if such responses might improve plant performance in the presence of the pathogen. Here, we conditioned soil by growing multiple generations (five) of Arabidopsis thaliana inoculated aboveground with Pseudomonas syringae pv tomato ( Pst) in the same soil. We then examined rhizosphere communities and plant performance in a subsequent generation (sixth) grown in pathogen-conditioned versus control-conditioned soil. Moreover, we assessed the role of altered root exudation profiles in shaping the root microbiome of infected plants.

          Results

          Plants grown in conditioned soil showed increased levels of jasmonic acid and improved disease resistance. Illumina Miseq 16S rRNA gene tag sequencing revealed that both rhizosphere and bulk soil bacterial communities were altered by Pst infection. Infected plants exhibited significantly higher exudation of amino acids, nucleotides, and long-chain organic acids (LCOAs) (C > 6) and lower exudation levels for sugars, alcohols, and short-chain organic acids (SCOAs) (C ≤ 6). Interestingly, addition of exogenous amino acids and LCOA also elicited a disease-suppressive response.

          Conclusion

          Collectively, our data suggest that plants can recruit beneficial rhizosphere communities via modification of plant exudation patterns in response to exposure to aboveground pathogens to the benefit of subsequent plant generations.

          Electronic supplementary material

          The online version of this article (10.1186/s40168-018-0537-x) contains supplementary material, which is available to authorized users.

          Related collections

          Most cited references24

          • Record: found
          • Abstract: found
          • Article: not found

          Induced systemic resistance by beneficial microbes.

          Beneficial microbes in the microbiome of plant roots improve plant health. Induced systemic resistance (ISR) emerged as an important mechanism by which selected plant growth-promoting bacteria and fungi in the rhizosphere prime the whole plant body for enhanced defense against a broad range of pathogens and insect herbivores. A wide variety of root-associated mutualists, including Pseudomonas, Bacillus, Trichoderma, and mycorrhiza species sensitize the plant immune system for enhanced defense without directly activating costly defenses. This review focuses on molecular processes at the interface between plant roots and ISR-eliciting mutualists, and on the progress in our understanding of ISR signaling and systemic defense priming. The central role of the root-specific transcription factor MYB72 in the onset of ISR and the role of phytohormones and defense regulatory proteins in the expression of ISR in aboveground plant parts are highlighted. Finally, the ecological function of ISR-inducing microbes in the root microbiome is discussed.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Feed Your Friends: Do Plant Exudates Shape the Root Microbiome?

            Plant health in natural environments depends on interactions with complex and dynamic communities comprising macro- and microorganisms. While many studies have provided insights into the composition of rhizosphere microbiomes (rhizobiomes), little is known about whether plants shape their rhizobiomes. Here, we discuss physiological factors of plants that may govern plant-microbe interactions, focusing on root physiology and the role of root exudates. Given that only a few plant transport proteins are known to be involved in root metabolite export, we suggest novel families putatively involved in this process. Finally, building off of the features discussed in this review, and in analogy to well-known symbioses, we elaborate on a possible sequence of events governing rhizobiome assembly.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Rhizosphere microbiome assemblage is affected by plant development.

              There is a concerted understanding of the ability of root exudates to influence the structure of rhizosphere microbial communities. However, our knowledge of the connection between plant development, root exudation and microbiome assemblage is limited. Here, we analyzed the structure of the rhizospheric bacterial community associated with Arabidopsis at four time points corresponding to distinct stages of plant development: seedling, vegetative, bolting and flowering. Overall, there were no significant differences in bacterial community structure, but we observed that the microbial community at the seedling stage was distinct from the other developmental time points. At a closer level, phylum such as Acidobacteria, Actinobacteria, Bacteroidetes, Cyanobacteria and specific genera within those phyla followed distinct patterns associated with plant development and root exudation. These results suggested that the plant can select a subset of microbes at different stages of development, presumably for specific functions. Accordingly, metatranscriptomics analysis of the rhizosphere microbiome revealed that 81 unique transcripts were significantly (P<0.05) expressed at different stages of plant development. For instance, genes involved in streptomycin synthesis were significantly induced at bolting and flowering stages, presumably for disease suppression. We surmise that plants secrete blends of compounds and specific phytochemicals in the root exudates that are differentially produced at distinct stages of development to help orchestrate rhizosphere microbiome assemblage.
                Bookmark

                Author and article information

                Contributors
                shenqirong@njau.edu.cn
                Journal
                Microbiome
                Microbiome
                Microbiome
                BioMed Central (London )
                2049-2618
                12 September 2018
                12 September 2018
                2018
                : 6
                : 156
                Affiliations
                [1 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, Jiangsu Provincial Key Lab for Organic Solid Waste Utilization; National Engineering Research Center for Organic-based Fertilizers; Jiangsu Collaborative Innovation Center for Solid Organic Waste Resource Utilization, , Nanjing Agricultural University, ; Nanjing, 210095 China
                [2 ]ISNI 0000 0001 0089 5711, GRID grid.260474.3, School of Geography Science, , Nanjing Normal University, ; Nanjing, 210021 China
                [3 ]ISNI 0000000120346234, GRID grid.5477.1, Plant-Microbe Interactions, Institute of Environmental Biology, , Utrecht University, ; Padualaan 8, 3584 CH Utrecht, the Netherlands
                [4 ]ISNI 0000000119573309, GRID grid.9227.e, State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, , Chinese Academy of Science, ; Beijing, 100101 China
                [5 ]ISNI 0000 0004 1936 8083, GRID grid.47894.36, Department of Horticulture and Landscape Architecture and Center for Rhizosphere Biology, , Colorado State University, ; Fort Collins, CO 80523 USA
                [6 ]ISNI 0000000120346234, GRID grid.5477.1, Ecology and Biodiversity Group, Department of Biology, Institute of Environmental Biology, , Utrecht University, ; Padualaan 8, 3584 CH Utrecht, the Netherlands
                Article
                537
                10.1186/s40168-018-0537-x
                6136170
                30208962
                7f916dbb-e6a5-4844-8969-9c6ed043764a
                © The Author(s). 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 25 May 2018
                : 23 August 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002855, Ministry of Science and Technology of the People's Republic of China;
                Award ID: 2015CB150500
                Award Recipient :
                Funded by: National Nature Science Foundation of China
                Award ID: 31330069
                Award Recipient :
                Funded by: National Postdoctoral Program for Innovative Talents
                Award ID: BX201600075
                Award Recipient :
                Funded by: Nature Science Foundation of Jiangsu Province
                Award ID: BK20170724
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                soil-borne legacy,foliar pathogen,microbiome,disease-suppressive soil,root exudates

                Comments

                Comment on this article